Using a model filamentous fungus to unravel mechanisms of lignocellulose deconstruction

Biotechnology for Biofuels

Elizabeth A Znameroski²  N Louise Glass¹ 

[1] Department of Plant and Microbial Biology, University of California, 94720, Berkeley, CA, USA

[2] Current address: Novozymes, 1445 Drew Avenue, 95618, Davis, CA, USA

关键词: Trichoderma;    Neurospora;    Secretome;    Transcriptome;    Filamentous fungus;    Lignocellulosic biofuels;    Cellulase;   

Others  :  798180
DOI  :  10.1186/1754-6834-6-6

 received in 2012-10-16, accepted in 2013-01-18,  发布年份 2013

【 摘 要 】

Filamentous fungi are the main source of enzymes used to degrade lignocellulose to fermentable sugars for the production of biofuels. While the most commonly used organism for the production of cellulases in an industrial setting is Trichoderma reesei (Hypocrea jecorina), recent work in the model filamentous fungus Neurospora crassa has shown that the variety of molecular, genetic and biochemical techniques developed for this organism can expedite analyses of the complexities involved in the utilization of lignocellulose as a source of carbon. These include elucidating regulatory networks associated with plant cell wall deconstruction, the identification of signaling molecules necessary for induction of the expression of genes encoding lignocellulolytic enzymes and the characterization of new cellulolytic enzymatic activities. In particular, the availability of a full genome deletion strain set for N. crassa has expedited high throughput screening for mutants that display a cellulolytic phenotype. This review summarizes the key findings of several recent studies using N. crassa to further understanding the mechanisms of plant cell wall deconstruction by filamentous fungi.

【 授权许可】

   
2013 Znameroski and Glass; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Field CB, Behrenfeld MJ, Randerson JT, Falkowski P: Primary production of the biosphere: integrating terrestrial and oceanic components. Science 1998, 281:237-240.
• [2]Carroll A, Somerville C: Cellulosic biofuels. Annu Rev Plant Biol 2009, 60:165-182.
• [3]Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD: Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 2007, 315:804-807.
• [4]Kubicek CP, Mikus M, Schuster A, Schmoll M, Seiboth B: Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol Biofuels 2009, 2:19.
• [5]Cherry JR, Fidantsef AL: Directed evolution of industrial enzymes: an update. Curr Opin Biotech 2003, 14:438-443.
• [6]Le Crom S, Schackwitz W, Pennacchio L, Magnuson JK, Culley DE, Collett JR, Martin J, Druzhinina IS, Mathis H, Monot F: Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing. Proc of the Natl Acad Sci USA 2009, 106:16151-16156.
• [7]Marsh PB, Bollenbacher K, Butler ML, Raper KB: The fungi concerned in fiber deterioration: II: their ability to decompose cellulose. Text Res J 1949, 19:462-484.
• [8]Eberhart BM, Beck RS, Goolsby KM: Cellulase of neurospora crassa. J Bacteriol 1977, 130:181-186.
• [9]Tian C, Beeson WT, Iavarone AT, Sun J, Marletta MA, Cate JH, Glass NL: Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc Natl Acad Sci USA 2009, 106:22157-22162.
• [10]Beadle GW, Tatum EL: Genetic control of biochemical reactions in neurospora. Proc Natl Acad Sci USA 1941, 27:499-506.
• [11]Hynes MJ: The Neurospora crassa genome open up the world of filamentous fungi. Genome Biol 2003, 4:217.
• [12]Dunlap JC, Borkovich KA, Henn MR, Turner GE, Sachs MS, Glass NL, McCluskey K, Plamann M, Galagan JE, Birren BW: Enabling a community to dissect an organism: overview of the neurospora functional genomics project. Adv Genet 2007, 57:49-96.
• [13]Luque EM, Gutierrez G, Navarro-Sampedro L, Olmedo M, Rodriguez-Romero J, Ruger-Herreros C, Tagua VG, Corrochano LM: A relationship between carotenoid accumulation and the distribution of species of the fungus Neurospora in Spain. PLoS One 2012, 7:e33658.
• [14]Galazka JM, Tian C, Beeson WT, Martinez B, Glass NL, Cate JH: Cellodextrin transport in yeast for improved biofuel production. Science 2010, 330:84-86.
• [15]Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S: The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422:859-868.
• [16]Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N: Lessons from the genome sequence of Neurospora crassa: Tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 2004, 68:1-108.
• [17]Znameroski EA, Coradetti ST, Roche CM, Tsai JC, Iavarone AT, Cate JH, Glass NL: Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc Natl Acad Sci USA 2012, 109:6012-6017.
• [18]Coradetti ST, Craig JP, Xiong Y, Shock T, Tian C, Glass NL: Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc Natl Acad Sci USA 2012, 109:7397-7402.
• [19]Ronne H: Glucose repression in fungi. Trends Genet 1995, 11:12-17.
• [20]Gancedo JM: Yeast carbon catabolite repression. Microbiol Mol Biol R 1998, 62:334-361.
• [21]Kostylev M, Wilson D: Synergistic interactions in cellulose hydrolysis. Biofuels 2011, 3:61-70.
• [22]Vaheri MP, Vaheri MEO, Kauppinen VS: Formation and release of cellulolytic enzymes during growth of Trichoderma reesei on cellobiose and glycerol. Eur J Appl Microbiol 1979, 8:73-80.
• [23]Chikamatsu G, Shirai K, Kato M, Kobayashi I, Tsukagoshi N: Structure and expression properties of the endo-beta-1,4-glucanase A gene from the filamentous fungus Aspergillus nidulans. FEMS Microbiol Lett 1999, 175:239-245.
• [24]Suzuki H, Igarashi K, Samejima M: Cellotriose and cellotetraose as inducers of the genes encoding cellobiohydrolases in the basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 2010, 76:6164-6170.
• [25]Sternberg D, Mandels GR: Induction of cellulolytic enzymes in Trichoderma reesei by sophorose. J Bacteriol 1979, 139:761-769.
• [26]Gielkens MM, Dekkers E, Visser J, de Graaff LH: Two cellobiohydrolase-encoding genes from Aspergillus niger require D-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl Environ Microbiol 1999, 65:4340-4345.
• [27]Aro N, Pakula T, Penttila M: Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 2005, 29:719-739.
• [28]Zhou Q, Xu J, Kou Y, Lv X, Zhang X, Zhao G, Zhang W, Chen G, Liu W: Differential involvement of beta-glucosidases from Hypocrea jecorina in rapid induction of cellulase genes by cellulose and cellobiose. Eukaryot Cell 2012, 11:1371-1381.
• [29]Kubicek CP, Messner R, Gruber F, Mandels M, Kubicek-Pranz EM: Triggering of cellulase biosynthesis by cellulose in Trichoderma reesei. Involvement of a constitutive, sophorose-inducible, glucose-inhibited beta-diglucoside permease. J Biol Chem 1993, 268:19364-19368.
• [30]Mandels M, Parrish FW, Reese ET: Sophorose as an inducer of cellulase in Trichoderma viride. J Bacteriol 1962, 83:400-408.
• [31]Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B: The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 2009, 37:D233-D238.
• [32]Sun J, Tian C, Diamond S, Glass NL: Deciphering transcriptional regulatory mechanisms associated with hemicellulose degradation in Neurospora crassa. Eukaryot Cell 2012, 11:482-493.
• [33]Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC: A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 2006, 103:10352-10357.
• [34]Brunner K, Lichtenauer AM, Kratochwill K, Delic M, Mach RL: Xyr1 regulates xylanase but not cellulase formation in the head blight fungus Fusarium graminearum. Curr Genet 2007, 52:213-220.
• [35]Calero-Nieto F, Di Pietro A, Roncero MI, Hera C: Role of the transcriptional activator xlnR of Fusarium oxysporum in regulation of xylanase genes and virulence. Mol Plant Microbe In 2007, 20:977-985.
• [36]Marui J, Kitamoto N, Kato M, Kobayashi T, Tsukagoshi N: Transcriptional activator, AoXlnR, mediates cellulose-inductive expression of the xylanolytic and cellulolytic genes in Aspergillus oryzae. FEBS Lett 2002, 528:279-282.
• [37]Stricker AR, Grosstessner-Hain K, Wurleitner E, Mach RL: Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot Cell 2006, 5:2128-2137.
• [38]Tsukagoshi N, Kobayashi T, Kato M: Regulation of the amylolytic and (hemi-) cellulolytic genes in aspergilli. J Gen Appl Microbiol 2001, 47:1-19.
• [39]Phillips CM, Iavarone AT, Marletta MA: A quantitative proteomic approach for cellulose degradation by Neurospora crassa. J Proteome Res 2011, 10:4177-4185.
• [40]Jun H, Kieselbach T, Jonsson LJ: Enzyme production by filamentous fungi: analysis of the secretome of Trichoderma reesei grown on unconventional carbon source. Microb Cell Fact 2011, 10:68.
• [41]Saykhedkar S, Ray A, Ayoubi-Canaan P, Hartson SD, Prade R, Mort AJ: A time course analysis of the extracellular proteome of Aspergillus nidulans growing on sorghum stover. Biotechnol Biofuels 2012, 5:52.
• [42]Adav SS, Ravindran A, Sze SK: Quantitative proteomic analysis of lignocellulolytic enzymes by Phanerochaete chrysosporium on different lignocellulosic substrates. J Proteomics 2012, 75:1493-1504.
• [43]Karlsson J, Saloheimo A, Siika-aho M, Tenkanen M, Penttila M, Tjerneld F: Homologous expression and characterization of Cel61A of Trichoderma reesei (EGIV). Eur J Biochem 2001, 258:6498-6507.
• [44]Beeson WT, Phillips CM, Cate JH, Marletta MA: Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J Am Chem Soc 2012, 134:890-892.
• [45]Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen JC, Johansen KS, Krogh KB, Jorgensen CI, Tovborg M, Anthonsen A: Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci USA 2011, 108:15079-15084.
• [46]Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG: Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 2012, 5:45.
• [47]Phillips CM, Beeson WT, Cate JH, Marletta MA: Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 2011, 6:1399-1406.
• [48]Davis RH: Neurospora: Contributions of a model organism. New York: Oxford University Press; 2000.
• [49]Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P: Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Nat Acad Sci USA 2009, 106:1954-1959.